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RNA-seq samples from male sex organs in Drosophila

ABSTRACT: Phenotypic evolution can result from gains and losses of genes, mutations in coding sequences, or regulatory mutations affecting gene expression. While the relative importance of these mechanisms is debated, regulatory evolution is recognized as a key driver of phenotypic diversity. In this study, we applied a phylogenetic model to discretized gene expression states (active or inactive) to investigate the evolutionary turnover of organ-specific transcriptomes, which we define as instances where gene expression is activated or deactivated in a particular organ. We focus on transcriptome turnover in two male reproductive organs in 11 species of the Drosophila melanogaster species group. Using the Bayesian inference method zigzag (Thompson et al. 2020), we estimate that testes express a higher proportion of the genome (65--75% of genes, depending on the species) compared to accessory glands (46--64%), with background expression noise producing less than 1% of transcripts in both organs. We find that many conserved genes have gained or lost expression in testes and accessory glands. Our model of joint transcriptome evolution, applied to 8,660 genes conserved as single copy families in all species (singleton genes), revealed similar turnover rates but distinct evolutionary trajectories in the two organs. We estimate that the genes in our data set transition between active and inactive expression states at rates on the order of 10^-9 yr^-1. The two organs experienced accelerated transcriptome turnover on different branches of the Drosophila phylogeny. The accessory glands exhibit greater variation in turnover rates among lineages, suggesting a lower baseline rate with bursts of rapid evolution in a subset of branches on the phylogeny. We do not observe significant differences in turnover rates between X-linked and autosomal genes. Genes that encode transcription factors transition between active and inactive states slower than non-TF genes in the accessory gland, but slightly faster in the testis. The results are robust to the choice of probability cut-offs used to discretize gene expression states, and there is good agreement between the estimates of expression states from zigzag and the inferences from the phylogenetic model. Overall, our study highlights the complex dynamics of transcriptome evolution in male reproductive organs. We discuss the benefits and challenges associated with investigating the evolution of gene expression as a binary trait and suggest potentially fruitful avenues for further methodological development.

ORGANISM(S): Drosophila elegans Drosophila ananassae Drosophila ficusphila Drosophila simulans Drosophila kikkawai Drosophila bipectinata Drosophila yakuba Drosophila eugracilis Drosophila takahashii Drosophila melanogaster Drosophila biarmipes

PROVIDER: GSE274048 | GEO | 2024/10/15

REPOSITORIES: GEO

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Project description:Male-derived accessory gland proteins (Acps) that are transferred to females during mating have profound effects on female reproductive physiology including increased ovulation, mating inhibition, and effects on sperm utilization and storage. The extreme rates of evolution seen in Acps may be driven by sperm competition and sexual conflict, processes which may ultimately drive complex interactions between female- and male-derived molecules and sperm. However, little is known of how gene expression in female reproductive tissues changes in response to the presence of male molecules and sperm. To characterize this response, we conducted parallel genomic and proteomic analyses of gene expression in the reproductive tract of 3-day-old unmated and mated female Drosophila melanogaster. Using DNA microarrays, we identified 539 transcripts that are differentially expressed in unmated vs. mated females and revealed a striking peak in differential expression at 6 hrs postmating and a marked shift from primarily down-regulated to primarily up-regulated transcripts within 3 hrs after mating. Combining two-dimensional gel electrophoresis and liquid chromatography mass spectrometry analyses, we identified 84 differentially expressed proteins at 3 hrs postmating, including proteins which appeared to undergo post-translational modification. Together, our observations define transcriptional and translational response to mating within the female reproductive tract and suggest a bimodal model of postmating gene expression initially correlated with mating and the final stages of female reproductive tract maturation and later with the declining presence of male reproductive molecules and with sperm maintenance and utilization. Experiment Overall Design: Three-day-old mated and unmated females were dissected to remove the lower reproductive tract (upper uterus, sperm-storage organs, and accessory glands). Mated females were dissected either immediately following mating (0 hr) or at 3, 6, or 24 hrs following the termination of mating. Tracts of 12-40 females of like category were pooled and total RNA extracted via a TRIzol-based protocol. Processing and labeling of transcript was performed by the Molecular Biology Core Facility at the Medical College of Georgia. Arrays from mated females at the different timepoints were compared to unmated females.

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RNA-seq samples from male sex organs in Drosophila

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